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Rapid evolution of a novel signalling mechanism by concerted duplication and divergence of a BMP ligand and its extracellular modulators

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Abstract

Gene duplication and divergence is widely considered to be a fundamental mechanism for generating evolutionary novelties. The Bone Morphogenetic Proteins (BMPs) are a diverse family of signalling molecules found in all metazoan genomes that have evolved by duplication and divergence from a small number of ancestral types. In the fruit fly Drosophila, there are three BMPs: Decapentaplegic (Dpp) and Glass bottom boat (Gbb), which are the orthologues of vertebrate BMP2/4 and BMP5/6/7/8, respectively, and Screw (Scw), which, at the sequence level, is equally divergent from Dpp and Gbb. It has recently been shown that Scw has arisen from a duplication of Gbb in the lineage leading to higher Diptera. We show that since this duplication event, Gbb has maintained the ancestral BMP5/6/7/8 functionality while Scw has rapidly diverged. The evolution of Scw was accompanied by duplication and divergence of a suite of extracellular regulators that continue to diverge together in the higher Diptera. In addition, Scw has become restricted in its receptor specificity: Gbb proteins can signal through the Type I receptors Thick veins (Tkv) and Saxophone (Sax), while Scw signals through Sax. Thus, in a relatively short span of evolutionary time, the duplication event that gave rise to Scw produced not only a novel ligand but also a novel signalling mode that is functionally distinct from the ancestral Gbb mode. Our results demonstrate the plasticity of the BMP pathway not only in evolving new family members and new functions but also new signalling modes by redeploying key regulators in the pathway.

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Acknowledgements

The authors would like to thank Claire Greer and James Patterson for their contributions to the early stages of this work and to the Drosophila Stock Centers, Malaria Research and Reference Reagent Resource, and the Drosophila Genome Resource Center for reagents. We are grateful to Wendy Gibson for providing Glossina morsitans, and Hazel Smith for the stalk-eyed flies Teleopsis dalmanni and Diasemopsis meigenii, Mark Wamalwa for access to the draft version of the G. morsitans genome, and Al Handler for access to the draft version of the C. capitata genome and Elio Sucena for performing the BLAST searches for Gbb and Scw. We would like to thank Hilary Ashe, Mark Dionne, Florian Maderspacher, and Stefan Thomsen for critical reading of the manuscript and to colleagues in the School of Life Sciences for helpful discussions. During the writing of this manuscript, C.F. was supported by a Wellcome Trust Programme Grant to Juan-Pablo Couso. The research was funded by grants from the Biotechnology and Biological Sciences Research Council (BB/C508050/1) and Medical Research Council (G0500916) to R.P.R.

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Authors and Affiliations

  1. School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG, United Kingdom

    Cornelia Fritsch & Robert P. Ray

  2. Centre for Macroevolution and Macroecology, Ecology Evolution and Genetics, Research School of Biology, Australian National University, Canberra, ACT, Australia

    Robert Lanfear

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  1. Cornelia Fritsch
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  2. Robert Lanfear
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Correspondence to Robert P. Ray.

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Communicated by: P. Simpson

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Fritsch, C., Lanfear, R. & Ray, R.P. Rapid evolution of a novel signalling mechanism by concerted duplication and divergence of a BMP ligand and its extracellular modulators. Dev Genes Evol 220, 235–250 (2010). https://doi.org/10.1007/s00427-010-0341-5

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